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Cited by 103Memory and Neural MechanismsSpatial Cognition and NavigationMemory Processes and Influences

Hippocampal and Retrosplenial Goal Distance Coding After Long-term Consolidation of a Real-World Environment

Open access
Patai, E Zita, Javadi, Amir-Homayoun, Ozubko, Jason D, O’Callaghan, Andrew, Ji, Shuman, Robin, Jessica, Grady, Cheryl, Winocur, Gordon +3 more·2019·Cerebral Cortex
DOI 10.1093/cercor/bhz044PMC PMC6519689

Published version of a preprint

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Abstract

Abstract Recent research indicates the hippocampus may code the distance to the goal during navigation of newly learned environments. It is unclear however, whether this also pertains to highly familiar environments where extensive systems-level consolidation is thought to have transformed mnemonic representations. Here we recorded fMRI while University College London and Imperial College London students navigated virtual simulations of their own familiar campus (> 2 years of exposure) and the other campus learned days before scanning. Posterior hippocampal activity tracked the proximity to the goal in the newly learned campus, but not in the familiar campus. By contrast retrosplenial cortex tracked the distance to the goal in the familiar campus, but not in the recently learned campus. These responses were abolished when participants were guided to their goal by external cues. These results open new avenues of research on navigation and consolidation of spatial information and help advance models of how neural circuits support navigation in novel and highly familiar environments. Significance Statement Historically, research on the hippocampal formation has focused on its role in long-term memory and navigation – often in isolation. No study to date has directly compared realistic navigation within familiar with recently learned environments, nor has it been explored how the neural substrates, along with computational codes, may change. In this study, we show for the first time, a shift from hippocampal to cortical coding of distance to a goal during active navigation. This study bridges the gap between memory consolidation and navigation, and paves the way for more functional and realistic understanding of the hippocampus.

AI snapshot

Written from the paper’s full text.

TL;DR

In a within-subject fMRI study, students navigated virtual simulations of their own long-familiar university campus and a campus learned days earlier. The right posterior hippocampus tracked goal distance in the recently learned campus and in familiar environments only when many turns lay ahead, whereas retrosplenial cortex tracked goal distance only in the familiar campus.

Key findings

  • During travel in the recently learned campus, right midposterior hippocampal activity showed a significant negative correlation with path distance to the goal, increasing with proximity to the goal; this was absent in the familiar campus and in control routes.
  • In the familiar campus, hippocampal activity showed a significant positive correlation with path distance, but only when the upcoming route contained many turns (≥3); there was no significant correlation with few turns (<3).
  • Retrosplenial cortex showed a significant positive correlation with path distance during travel in the familiar campus, greatest when participants were farthest from the goal; this was absent in the recent campus and control conditions.
  • Behaviorally, participants were more accurate at decision points in the familiar campus (M = 89.9%, SD = 11%) than the recent campus (M = 80.4%, SD = 13%; t[24] = 3.6, P = 0.002) and responded faster in the familiar campus (1.19 ± 0.4 s vs. 1.39 ± 0.5 s; t[24] = −4.7, P < 0.001). They reported more planning at decision points in the recent environment (22%) than the familiar environment (8%; t < −2.9, P < 0.006).

Methods

  • Final sample: 25 students (12 UCL, 13 Imperial; mean age 23 years, range 20–26; 12 males, 13 females) who had studied at their own campus for at least 2 years and had little or no familiarity with the other campus.
  • Participants learned 10 goal locations, 18 streets, and 8 start points in both environments, including a guided real-world tour of both campuses in the days before scanning; fMRI used virtual Google Street View-based routes with active navigation and control “follow” blocks.
  • fMRI analysis used SPM12 with a priori small-volume correction masks for right mid/posterior hippocampus and retrosplenial cortex; path distance, Euclidean distance, and egocentric goal direction were modeled as parametric regressors, with focus on Travel Periods and Decision Points.

Limitations

  • The paper states that scanner coverage made it impossible to assess entorhinal cortex contributions to distance coding, unlike Howard et al. (2014).
  • The paper states that ecological validity required lower trial numbers per condition, though the two main periods of interest had >20 events per condition; control analyses separating travel midpoints replicated the hippocampal effect only with mid-hippocampal small-volume correction and did not replicate the retrosplenial effect, instead finding precuneus/parietal–occipital sulcus effects.
  • Evident from the text: the study used a modest sample (n = 25), a 1.5 T scanner, virtual rather than real-world navigation, and only two campus environments; path distance and Euclidean distance were highly correlated, and the authors note that environment structure, size, and visual detail may influence the direction of hippocampal goal-distance coding.

Model-written summary. Check it against the paper before relying on it.

Integrity signals

Registry

Crossref · 10.1093/cercor/bhz044

Cites

74 of 74 references verified0 citation errors · 0 not checkable

Statistics

Nothing to recompute.

Claims the paper makes

0 of 48 cited sources checked · 0 supported · 0 flagged

  • Findingown data

    The hippocampal and retrosplenial distance-to-goal responses were abolished when participants were guided to their goal by external cues.

    “All of these responses were abolished when participants were guided to their goal by external cues.”
    Quote in the paperSubstantial claim
    • Rests on an assumption: The crucial difference between the familiar and recent environments was the long-term (>2 year) prior knowledge of one campus, after both campuses were intensively trained in the preceding days.
  • Findingown data

    There was no correlation between planning and accuracy (all r > −0.16, P > 0.1).

    “However, there was no correlation between planning and accuracy (all r>−0.16, P > 0.1).”
    Quote in the paperNot a substantial claim
    • Rests on an assumption: Participants' debriefing reports accurately reflect their planning during scanning.
  • Findingown data

    Posterior hippocampal activity tracked the distance to the goal in the newly learned campus.

    “Posterior hippocampal activity tracked the distance to the goal in the newly learned campus”
    Quote in the paperSubstantial claim
    • Rests on an assumption: The crucial difference between the familiar and recent environments was the long-term (>2 year) prior knowledge of one campus, after both campuses were intensively trained in the preceding days.
  • Findingown data

    There were no clear differences when comparing familiar to recent navigation.

    “There were no clear differences when comparing familiar to recent navigation (Fig. S2 and Supplementary Results).”
    Quote in the paperNot a substantial claim
  • Findingown data

    Posterior hippocampal activity tracked the distance to the goal in familiar environments when the future route contained many turns.

    “as well as in familiar environments when the future route contained many turns”
    Quote in the paperSubstantial claim
    • Rests on an assumption: The crucial difference between the familiar and recent environments was the long-term (>2 year) prior knowledge of one campus, after both campuses were intensively trained in the preceding days.
  • May combine two claims. 28
  • Classified as probably not a substantial claim. 25
  • The quote only partly states this claim. 1

  • May combine two claims.

    Findingown data

    In the pre-training assessment, participants in the familiar environment were on average 48% accurate on street names and 86% accurate on landmarks.

    “In the familiar environment participants were on average 48% and 86% accurate on street names and landmarks, respectively.”
    Quote in the paperSubstantial claim

  • May combine two claims.

    Findingown data

    There was a significant effect of environment, type of information probed, and their interaction on pre-training assessment accuracy.

    “Thus, there was a significant effect of environment (F[1,24] = 140.8,P < 0.001), type of information probed (F[1,24] = 48.9,P < 0.001), and interaction (F[1,24] = 14.8, P = 0.001).”
    Quote in the paperSubstantial claim

  • May combine two claims.

    Findingown data

    Participants were able to orient themselves and make correct decisions at Decision Points in both environments, albeit better in their familiar campus.

    “Behavioral results revealed that participants were able to orient themselves and make correct decisions at Decision Points in both environments, albeit better so in their familiar campus”
    Quote in the paperSubstantial claim

  • May combine two claims.

    Findingown data

    Familiar campus accuracy at Decision Points was M = 89.9%, SD = 11%; recent campus accuracy was M = 80.4%, SD = 13%; paired t[24] = 3.6, P = 0.002.

    “Familiar: M = 89.9%, SD = 11%; Recent: M = 80.4%, SD = 13%, paired sample t-test: t[24] = 3.6, P = 0.002”
    Quote in the paperSubstantial claim

  • May combine two claims.

    Findingown data

    There was no correlation between SBSDS and NSQ scores, between these scores and performance in the scanner, or to the amount of planning reported.

    “There was no correlation between the scores on these 2 questionnaires, between these scores and performance in the scanner, or to the amount of planning reported.”
    Quote in the paperNot a substantial claim

  • May combine two claims.

    Findingown data

    A categorical analysis revealed more activity in lateral and medial parietal areas in familiar environments when actively navigating compared with just following along a route, whereas recent environments did not show such a distinction.

    “A categorical analysis of different event types and task blocks revealed more activity in lateral and medial parietal areas in familiar environments when actively navigating (“navigation” condition) compared with just following along a route (“control” condition), whereas recent environments did not show such a distinction (Fig. S1).”
    Quote in the paperNot a substantial claim

  • May combine two claims.

    Findingown data

    In the pre-training assessment, participants in the recent campus were on average 10% accurate on street names and 22% accurate on landmarks.

    “Conversely, for the recent campus, they were only 10% accurate on the street names, and 22% for landmarks.”
    Quote in the paperSubstantial claim

  • May combine two claims.

    Findingown data

    When examining Travel midpoints only, the right hippocampal effect in recent navigation was replicated, though it only survived a mid-hippocampal small-volume correction.

    “When examining Travel midpoints only, we replicated the right hippocampal effect in recent navigation, though this only survived a mid-hippocampal SVC (Table S4)”
    Quote in the paperNot a substantial claim

  • May combine two claims.

    Findingown data

    There was no significant correlation between hippocampal activity and path distance when there were few turns (<3) in familiar environments or either type of Travel event in recent environments or during control routes.

    “There was no significant correlation between hippocampal activity and path distance when there were few turns (<3) in familiar environments or either type of Travel event in the recent environments or during the control routes.”
    Quote in the paperSubstantial claim

  • May combine two claims.

    Findingown data

    When examining Travel midpoints only, the retrosplenial cortex effect in familiar navigation routes was not replicated, but there was a positive correlation of path distance in the precuneus and parietal-occipital sulcus.

    “however we did not replicate the retrosplenial cortex in familiar navigation routes, but there was a positive correlation of PD in the precuneus and parietal–occipital sulcus (Table S4).”
    Quote in the paperNot a substantial claim

  • May combine two claims.

    Findingown data

    While Howard et al. (2014) found a positive correlation between posterior right hippocampal activity and distance, the present study observed a negative correlation in recently learned environments.

    “However, while Howard et al. (2014) found a positive correlation between posterior right hippocampal activity and distance, we observed a negative correlation in the recently learned environments.”
    Quote in the paperSubstantial claim0 of 1 sources checked
    • cites Howard et al. 2014 source

      Not checked in the free run.

  • May combine two claims.

    Findingown data

    During navigation in recent environments, mid hippocampus was more active the further away and less directly ahead the goal was.

    “During the navigation task in recent environments we found the mid hippocampus was more active the further away, and less directly ahead the goal was (see Table S4 for details of activation).”
    Quote in the paperSubstantial claim

  • Classified as probably not a substantial claim.

    Premisecitation

    In recently learned environments, the hippocampus has been shown to encode the distance to the goal.

    “In recently learned environments, the hippocampus has been shown to encode the distance to the goal (Spiers and Maguire 2007b; Viard et al. 2011; Sherrill et al. 2013; Howard et al. 2014; Chrastil et al. 2015; Balaguer et al. 2016; Spiers et al. 2017)”
    Quote in the paperSubstantial claim0 of 3 sources checked
    • cites Spiers and Maguire 2007b

      Not checked in the free run.

    • cites Viard et al. 2011 source

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    • cites Sherrill et al. 2013 source

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  • May combine two claims.

    Interpretationown data

    Participants had better knowledge about their own campus, and mainly its landmarks.

    “underscoring the notion that participants did indeed have better knowledge about their own campus, and mainly its landmarks.”
    Quote in the paperSubstantial claim

  • Classified as probably not a substantial claim.

    Premisecitation

    Candidate neocortical regions for coding such information include the retrosplenial cortex, parahippocampal cortex, and anterior cingulate cortex.

    “Candidate neocortical regions include the retrosplenial cortex (Takahashi et al. 1997; Epstein et al. 2007), parahippocampal cortex (Rosenbaum et al. 2004; Bohbot et al. (2015), for extensive reviews see Spiers and Maguire 2007b; Epstein 2008; Ranganath and Ritchey 2012; Miller et al. 2014), and the anterior cingulate cortex (Teixeira et al. 2006).”
    Quote in the paperSubstantial claim0 of 3 sources checked
    • cites Takahashi et al. 1997 source

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    • cites Epstein et al. 2007 source

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    • cites Rosenbaum et al. 2004 source

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  • Classified as probably not a substantial claim.

    Study design and conductreasoning

    The order in which participants were trained on the campuses was counterbalanced across participants and familiarity.

    “The order in which participants were trained on the campuses was counterbalanced across participants and familiarity”
    Quote in the paperSubstantial claim

  • Probably not a substantial claim: may not pass S3 (load-bearing). May combine two claims.

    Study design and conductnone given

    The order of routes within campuses was counterbalanced, while navigation and control conditions, or routes between campuses, were interleaved across participants.

    “The order of routes within campuses was counterbalanced, while either navigation and control conditions, or routes between campuses were interleaved across participants.”
    Quote in the paperNot a substantial claim

  • Classified as probably not a substantial claim.

    Premisecitation

    Current models argue that through systems consolidation, neocortical regions may come to code distance/direction information in extensively learned environments.

    “Current models argue that through systems consolidation, neocortical regions may come to code such information in extensively learned environments (Spiers and Maguire 2007b).”
    Quote in the paperSubstantial claim0 of 1 sources checked
    • cites Spiers and Maguire 2007b

      Not checked in the free run.

  • Classified as probably not a substantial claim. May combine two claims.

    Study design and conductreasoning

    The training order was counterbalanced to ensure that the familiar campus was also recently visited in its entirety, thereby removing confounding effects of recency of exposure rather than age of memory.

    “The order in which participants were trained on the campuses was counterbalanced across participants and familiarity, and was done to ensure that the familiar campus was also recently visited in its entirety, thereby removing any confounding effects of just the recency of exposure (rather than the age of the memory itself).”
    Quote in the paperSubstantial claim

  • Probably not a substantial claim: may not pass S1 (asserted). May combine two claims.

    Premisecitation

    SCT argues that initially the hippocampus is involved in processing spatial memories, and that over time representations in neocortical regions are strengthened, reducing the demand on the hippocampus.

    “the standard consolidation theory (SCT) argues that initially the hippocampus is involved in processing the spatial memories, and that over time the representations in neocortical regions are strengthened, reducing the demand on the hippocampus (Squire 1992; Squire and Zola-Morgan 1998).”
    Quote in the paperNot a substantial claim0 of 2 sources checked
    • cites Squire 1992 source

      Not checked in the free run.

    • cites Squire and Zola-Morgan 1998

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  • May combine two claims.

    Premisecitation

    A subsequent longitudinal fMRI study showed that participants newly arrived to a city initially relied on the hippocampus for navigation but after 6 months could navigate without evidence of hippocampal involvement.

    “In a subsequent longitudinal, fMRI study, Hirshhorn, Grady, Rosenbaum, Winocur, and Moscovitch (2012) showed that participants who were newly arrived to a city, initially relied on the hippocampus for navigation but after 6 months could navigate without evidence of hippocampal involvement.”
    Quote in the paperSubstantial claim0 of 1 sources checked
    • cites Hirshhorn, Grady, Rosenbaum, Winocur, and Moscovitch (2012)

      Not checked in the free run.

  • Probably not a substantial claim: may not pass S3 (load-bearing).

    Premisecitation

    One prior fMRI study involving London taxi drivers navigating a virtual simulation of London reported that the hippocampus is engaged at the start of navigating this highly familiar environment.

    “One study involving London taxi drivers navigating a virtual simulation of London (UK) reported that the hippocampus is engaged at the start of navigating this highly familiar environment (Spiers and Maguire 2006).”
    Quote in the paperNot a substantial claim0 of 1 sources checked
    • cites Spiers and Maguire 2006 source

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  • Probably not a substantial claim: may not pass S3 (load-bearing).

    Premisecitation

    MTT/TTT predicts that the hippocampus, and in particular the posterior hippocampus, would play a more important role if detailed processing is required.

    “with MTT/TTT predicting that the hippocampus, and in particular the posterior hippocampus, would play a more important role if detailed processing is required (Poppenk et al. 2013).”
    Quote in the paperNot a substantial claim0 of 1 sources checked
    • cites Poppenk et al. 2013 source

      Not checked in the free run.

  • Probably not a substantial claim: may not pass S3 (load-bearing).

    Study design and conductnone given

    No participants had any abrupt motion changes over 4 mm.

    “No participants had any abrupt motion changes over 4 mm.”
    Quote in the paperNot a substantial claim

  • Probably not a substantial claim: may not pass S3 (load-bearing). May combine two claims.

    Study design and conductreasoning

    Path distance was entered independently as a parametric regressor in analyses, and results were checked when including ED along with PD to establish robustness.

    “Therefore, we entered path distance independently as a parametric regressor in our analyses, as this was the main focus of our task. However, we also checked our results when including ED along with PD, to establish the robustness of our findings, even with highly correlated regressors.”
    Quote in the paperNot a substantial claim

  • May combine two claims. The quote only partly states this claim.

    Study design and conductown data

    Including Euclidean distance in the models investigating parametric effects of path distance replicated the path distance results, and all effects survive small-volume correction including when ED is added.

    “We included ED in the models investigating parametric effects of PD. We replicated the PD results, emphasizing the robustness of these effects (see Table S4), despite highly correlated parametric regressors (see Table S1).”
    Quote in the paperNot a substantial claim

  • Probably not a substantial claim: may not pass S3 (load-bearing).

    Study design and conductnone given

    All results reported are displayed at P = 0.005 uncorrected.

    “All results reported are displayed at P = 0.005 uncorrected”
    Quote in the paperNot a substantial claim

  • Probably not a substantial claim: may not pass S3 (load-bearing).

    Study design and conductcitation

    The hippocampus mask was a combination of right mid and posterior sections, a priori based on Howard et al. 2014.

    “The hippocampus mask was a combination of right mid and posterior sections (a priori based on the results of Howard et al. 2014).”
    Quote in the paperNot a substantial claim0 of 1 sources checked
    • cites Howard et al. 2014 source

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  • Probably not a substantial claim: may not pass S3 (load-bearing). May combine two claims.

    Study design and conductown data

    One participant was excluded due to below chance performance during the fMRI session, resulting in a final sample of 25 subjects.

    “We collected 26 datasets, but one participant was excluded due to below chance performance during the fMRI session, resulting in the final sample of 25 subjects”
    Quote in the paperNot a substantial claim

  • Classified as probably not a substantial claim.

    Study design and conductnone given

    Small-volume correction (P < 0.05) was performed using anatomical masks.

    “Small-volume correction (P < 0.05) was performed using anatomical masks (as described in detail in the Methods section).”
    Quote in the paperSubstantial claim

  • Probably not a substantial claim: may not pass S3 (load-bearing).

    Study design and conductnone given

    The retrosplenial mask was based on the anatomical retrosplenial cortex specifically (BA 29/30).

    “The retrosplenial mask was based on the anatomical restrosplenial cortex specifically (BA 29/30).”
    Quote in the paperNot a substantial claim

  • Probably not a substantial claim: may not pass S3 (load-bearing).

    Study design and conductreasoning

    A trial-by-trial inverse efficiency score (RT/mean accuracy) was included as a regressor when modeling Decision Points to control for potential differences in brain activation due to reaction time differences in the familiarity condition.

    “To control for potential differences in brain activation due to reaction time differences in the familiarity condition, we included a trial-by-trial inverse efficiency score (RT/mean accuracy) as a regressor when modeling the Decision Points.”
    Quote in the paperNot a substantial claim

  • Probably not a substantial claim: may not pass S3 (load-bearing).

    Study design and conductreasoning

    The scan coverage made it impossible to assess the contribution of the entorhinal cortex to the coding of distance.

    “making it impossible to assess the contribution of the entorhinal cortex to the coding of distance, as was reported in Howard et al.”
    Quote in the paperNot a substantial claim0 of 1 sources checked
    • cites Howard et al.

      Not checked in the free run.

  • May combine two claims.

    Premisecitation

    Distance tracking is not automatic and requires goal-directed navigation.

    “such distance tracking is not automatic and requires goal-directed navigation.”
    Quote in the paperSubstantial claim0 of 1 sources checked
    • cites Howard et al. 2014 source

      Not checked in the free run.

  • May combine two claims.

    Interpretationown data

    The correlation of hippocampal activity to distance to goal during travel periods in recently learned environment agrees with prior fMRI reports of similar coding and supports models which argue the hippocampus computes information about the future path to goal for navigational guidance.

    “The correlation of hippocampal activity to distance to goal during travel periods in navigation routes in the recently learned environment agrees with prior fMRI reports of similar coding (Viard et al. 2011; Sherrill et al. 2013; Howard et al. 2014; Balaguer et al. 2016) and supports models which argue the hippocampus computes information about the future path to goal for navigational guidance (Er”
    Quote in the paperSubstantial claim0 of 3 sources checked
    • cites Viard et al. 2011 source

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    • cites Sherrill et al. 2013 source

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    • cites Howard et al. 2014 source

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  • Probably not a substantial claim: may not pass S3 (load-bearing).

    Study design and conductown data

    Two subjects did not have segments long enough for the goal-straight-ahead analysis and were excluded.

    “Two subjects did not have segments long enough (this depended on the routes they were given and some routes had shorter “goal approach” segments) and were not included in the analysis.”
    Quote in the paperNot a substantial claim

  • May combine two claims.

    Interpretationown data

    The present study observed evidence for continued hippocampal engagement in an environment learned 2 years prior to testing, which is at odds with SCT.

    “Firstly, we observed evidence for continued hippocampal engagement in an environment learned 2 years prior to testing, which is at odds with SCT.”
    Quote in the paperSubstantial claim

  • Probably not a substantial claim: may not pass S3 (load-bearing). May combine two claims.

    Premisecitation

    Recent evidence indicates that turns in a path and familiarity with an environment can impact representations of distance.

    “Recent evidence indicates that turns in a path and the familiarity with an environment can also impact on representations of distance (Bonasia et al. 2016; Jafarpour and Spiers 2016; Brunec et al. 2017).”
    Quote in the paperNot a substantial claim0 of 3 sources checked
    • cites Bonasia et al. 2016 source

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    • cites Jafarpour and Spiers 2016 source

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    • cites Brunec et al. 2017 source

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  • Classified as probably not a substantial claim.

    Premisecitation

    It has remained unclear which brain regions are responsible for spatial processing in highly familiar environments.

    “It has remained unclear which brain regions are responsible for spatial processing in highly familiar environments (Spiers and Maguire 2007b).”
    Quote in the paperSubstantial claim0 of 1 sources checked
    • cites Spiers and Maguire 2007b

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  • Probably not a substantial claim: may not pass S3 (load-bearing).

    Premisecitation

    Prior neuropsychological research has consistently indicated the dominance of the right hemisphere in processing spatial information.

    “Prior neuropsychological research has consistently indicated the dominance of the right hemisphere in processing spatial information (Spiers et al. 2001; Burgess et al. 2001, 2002)”
    Quote in the paperNot a substantial claim0 of 3 sources checked
    • cites Spiers et al. 2001 source

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    • cites Burgess et al. 2001 source

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    • cites Burgess et al. 2002 source

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  • Probably not a substantial claim: may not pass S3 (load-bearing).

    Interpretationcitation

    The present findings are broadly consistent with fMRI evidence that retrosplenial cortex activity is positively correlated with distance back to the start of a simple circular journey.

    “Our findings are broadly consistent with fMRI evidence that retrosplenial cortex activity is positively correlated with the distance back to the start of a simple circular journey (Chrastil et al. 2015).”
    Quote in the paperNot a substantial claim0 of 1 sources checked
    • cites Chrastil et al. 2015 source

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  • May combine two claims.

    Interpretationown data

    The present study found a transformation in the direction of the correlation between the hippocampus and distance to the goal during travel periods when familiar environments were compared with recently learned environments; this reversal suggests that the computations and/or type of information represented in the hippocampus changes with consolidation.

    “Secondly, we found a transformation in the direction of the correlation between the hippocampus and the distance to the goal during travel periods when familiar environments were compared with recently learned environment. This reversal suggests that the computations and/or the type of information that is represented in the hippocampus changes with consolidation.”
    Quote in the paperSubstantial claim

  • Classified as probably not a substantial claim. May combine two claims.

    Premisecitation

    Dominant accounts of memory consolidation, SCT and MTT/TTT, both claim that with passage of time and experience, performance on some tasks becomes independent of the hippocampus and comes to rely on extra-hippocampal structures such as the retrosplenial cortex.

    “Dominant accounts of memory consolidation, SCT, and MTT/TTT, both claim that with the passage of time and experience, performance on some tasks becomes independent of the hippocampus and comes to rely on extra-hippocampal structures such as the retrosplenial cortex (Marr 1971; Alvarez and Squire 1994; Frankland and Bontempi 2005; Winocur and Moscovitch 2011; Sekeres et al. 2018).”
    Quote in the paperSubstantial claim0 of 3 sources checked
    • cites Marr 1971 source

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    • cites Alvarez and Squire 1994

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    • cites Frankland and Bontempi 2005 source

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  • Classified as probably not a substantial claim.

    Premisecitation

    The retrosplenial cortex has been posited as supporting long-term spatial knowledge.

    “One brain region posited as supporting this long-term knowledge has been the retrosplenial cortex (Spiers and Maguire 2007b).”
    Quote in the paperSubstantial claim0 of 1 sources checked
    • cites Spiers and Maguire 2007b

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  • May combine two claims.

    Interpretationcitation

    The observation that retrosplenial cortex only comes to code distance to goal after extended experience with the environment is consistent with several past studies which have observed increased activity in retrosplenial cortex with acquisition of spatial knowledge.

    “Our observation that retrosplenial cortex only comes to code the distance to the goal after extended experience with the environment is consistent with several past studies which have observed increased activity in the retrosplenial cortex with the acquisition of spatial knowledge about an environment (Wolbers and Büchel 2005; Auger et al. 2012, 2015).”
    Quote in the paperNot a substantial claim0 of 3 sources checked
    • cites Wolbers and Büchel 2005

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    • cites Auger et al. 2012 source

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    • cites Auger et al. 2015

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  • May combine two claims.

    Interpretationown data

    The present data supports models in which there is change in demand on brain regions with extended consolidation of memories of an environment, with retrosplenial cortex specifically tracking distance to goal in familiar environments and hippocampus tracking goal distance in recent environments and also familiar environments when future route contains many turns.

    “Our data supports models in which there is change in demand on brain regions with extended consolidation of the memories of an environment, with the retrosplenial cortex specifically tracking the distance to the goal in familiar environments and the hippocampus tracking goal distance in recent environments and also familiar environments when the future route contains many turns.”
    Quote in the paperSubstantial claim
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  • The paper relies on this without support.

    The crucial difference between the familiar and recent environments was the long-term (>2 year) prior knowledge of one campus, after both campuses were intensively trained in the preceding days.

    “ensuring that the crucial difference between the 2 environments was the long-term (>2 year) prior knowledge of one of them.”

  • The paper relies on this without support.

    The virtual simulation of the campuses using Google Maps Street View panoramas is a valid model of real-world navigation that engages the same spatial representations as real-world navigation.

    “The task in the scanner was designed to simulate walking through the campuses, by using panorama images from Google Maps Street View”

  • The paper relies on this without support.

    Extensive systems-level consolidation has transformed mnemonic representations in highly familiar environments.

    “where extensive systems-level consolidation is thought to have transformed mnemonic representations.”

  • The paper relies on this without support.

    Participants' debriefing reports accurately reflect their planning during scanning.

    “Participants were instructed to report what they remembered thinking during the navigation, not what they should have done”

  • The paper relies on this without support.

    The environment used by Howard et al. (2014) contained more junctions than the environments used in the present study, so most routes in that study likely required many turns.

    “Notably, the environment used by Howard et al. (2014) (Soho, London, UK) contained more junctions to navigate across compared with the environments we used, thus most routes examined would likely have required many turns.”

  • The paper relies on this without support.

    Soho contains many more distinct landmarks than the campuses used in the present study.

    “Soho contains many more distinct landmarks than the campuses we used.”
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Claims other papers make about this one

Each is checked against this paper’s own text: does it say what the citing paper says it does?

  • Such a representation might take a schematic form, such that similar distances across different environments are processed similarly or by the same neural populations in the RSC.

    “Such a representation might take a schematic form, such that similar distances across different environments are processed similarly or by the same neural populations in the RSC 153,154 .”

    From From cognitive maps to spatial schemas (2023) · cites this paper as [153]

  • In our recent research, the RSC was found to code distance to goals in well-known, real-world environments, but not in recently learned environments.

    “In our recent research, the RSC was found to code distance to goals in well-known, real-world environments, but not in recently learned environments 153 .”

    From From cognitive maps to spatial schemas (2023) · cites this paper as [153]

Self-check

Percentages, sums and reported differences re-computed from the paper’s own numbers.

Each contradiction between two passages listed here was confirmed by an independent check.

  • Some routes had only one new goal event

    Minor

    The paper says each route had multiple new goal locations, but the reported range includes routes with just one new goal event.

1 of 1

Cites

Flagged first, then by citations

1 of the 75 references couldn’t be matched to a known paper.

Research works printed but not linked: 1

  1. Tulving, 1998, Episodic and declarative memory: role of the hippocampus, Hippocampus, 8, 198, 10.1002/(sici)1098-1063(1998)8:3<198::aid-hipo2>3.0.co;2-g · DOI · Paper page

Cited by

Sorted by citations

Related

Authors
Patai, E. Z., Javadi, A.-H., Ozubko, J. D., O’Callaghan, A., Ji, S., Robin, J., Grady, C., Winocur, G., Rosenbaum, R. S., Moscovitch, M., & Spiers, H. J.
Affiliations
  • University College London (GB)
  • University of Kent (GB)
  • SUNY Geneseo (US)
  • University of Toronto (CA)
  • York University (CA)
Corresponding author
Spiers, Hugo J
ORCID
Venue
Cerebral Cortex
Publisher
Oxford University Press (OUP)
Published
2019-02-20
Volume
29
Issue
6
Pages
2748-2758
ISSN
  • 1047-3211 (ISSN-L)
  • 1460-2199
DOI
10.1093/cercor/bhz044
PMC
PMC6519689
OpenAlex
W2923481172
Cited by
102
References
75
Citations by year
2026: 10 · 2025: 11 · 2024: 17 · 2023: 14 · 2022: 12 · 2021: 15 · 2020: 9 · 2019: 6 · 2018: 5 · 2017: 3
FWCI
6.11
Type
journal article
Language
en
Open access
Licence
Locations
  • Cerebral Cortex (publishedVersion, cc-by)
  • bioRxiv (Cold Spring Harbor Laboratory) (acceptedVersion)
  • PubMed Central (publishedVersion, cc-by)
  • PubMed (publishedVersion)
  • Kent Academic Repository (University of Kent) (submittedVersion)
  • UCL Discovery (University College London) (submittedVersion)
Funders
  • HJS
  • James S. McDonnell Foundation
  • Canadian Institute of Health Research (# 49566)
  • MM and SR
Topics
  • Life Sciences › Neuroscience › Cognitive Neuroscience › Memory and Neural Mechanisms
  • Physical Sciences › Engineering › Automotive Engineering › Spatial Cognition and Navigation
  • Life Sciences › Neuroscience › Cognitive Neuroscience › Memory Processes and Influences
Keywords
hippocampus, retrosplenial cortex, spatial navigation, systems consolidation, familiar environment, virtual navigation, external cues, route complexity, spatial memory
MeSH terms
Brain Mapping, Female, Goals, Hippocampus, Humans, Magnetic Resonance Imaging, Male, Temporal Lobe, Young Adult, Spatial Memory, Spatial Learning, Spatial Navigation

About these checks

Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.

Claims read by deepseek-v4.1-flash under definition version 3 (extract-v3) on 2026-10-09.

Classified by jev-1.13-20260917 (gold-guideline-v0.2) on 2026-10-09.

Statistics and arithmetic are recomputed, not judged.

Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.

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